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Bone-adiposity cross-talk: implications for pediatric obesity

A narrative review of literature

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Abstract

The rising prevalence of overweight and obesity among pediatric populations has become a major global concern. The objective of this review is to demonstrate potential interactions between the products released by fat tissue and the hormonal production of bone tissue in obese children and adolescents. Advancing the understanding of the complex interactions between adipocyte and osteocyte activities may contribute to the mechanistic understanding of the body’s responses to weight loss during adolescence. This knowledge could also reveal any side effects encountered with these interventions. Currently, the concept of bone-adiposity crosstalk has not been fully elucidated, and the mechanisms remain controversial. Understanding the local interactions between the released products by fat tissue and hormones produced in bone tissue requires further investigations.

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References

  1. WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894:i–xii, 1–253

  2. Mosca LN, da Silva VN, Goldberg TB (2013) Does excess weight interfere with bone mass accumulation during adolescence? Nutrients 5:2047–2061

    Article  PubMed Central  PubMed  Google Scholar 

  3. Ng M et al (2014) Global, regional, and national prevalence of overweight and obesity in children and adults during 1980–2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384:766–781

    Article  PubMed  Google Scholar 

  4. Daniels S (2009) Complications of obesity in children and adolescents. Int J Obes 33:S60–S65

    Article  Google Scholar 

  5. Frost H (1987) Bone “mass” and the “mechanostat”: a proposal. Anat Rec 219:1–9

    Article  CAS  PubMed  Google Scholar 

  6. Goulding A et al (2000) Overweight and obese children have low bone mass and area for their weight. Int J Obes Relat Metab Disord 24:627–632

    Article  CAS  PubMed  Google Scholar 

  7. Goulding A, Grant AM, Williams SM (2005) Bone and body composition of children and adolescents with repeated forearm fractures. J Bone Miner Res 20:2090–2096

    Article  PubMed  Google Scholar 

  8. Shapses SA, Sukumar D (2012) Bone metabolism in obesity and weight loss. Annu Rev Nutr 32:287–309

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Frost HM (2003) Bone’s mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081–1101

    Article  PubMed  Google Scholar 

  10. Karsenty G (2006) Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 4:341–348

    Article  CAS  PubMed  Google Scholar 

  11. Lee NK et al (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Júnior IF et al (2013) The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents. BMC Pediatr 13:37

    Article  PubMed Central  PubMed  Google Scholar 

  13. Russell M et al (2010) Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab 95:1247–1255

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Klein KO et al (1998) Effect of obesity on estradiol level, and its relationship to leptin, bone maturation, and bone mineral density in children. J Clin Endocrinol Metab 83:3469–3475

    Article  CAS  PubMed  Google Scholar 

  15. Rocher E et al (2008) Bone mineral density in prepubertal obese and control children: relation to body weight, lean mass, and fat mass. J Bone Miner Metab 26:73–78

    Article  PubMed  Google Scholar 

  16. Dimitri P, Wales JK, Bishop N (2010) Fat and bone in children: differential effects of obesity on bone size and mass according to fracture history. J Bone Miner Res 25:527–536

    Article  PubMed  Google Scholar 

  17. Ellis K et al (2003) Bone mineral mass in overweight and obese children: diminished or enhanced? Acta Diabetol 40:s274–s277

    Article  PubMed  Google Scholar 

  18. Leonard MB et al (2004) Obesity during childhood and adolescence augments bone mass and bone dimensions. Am J Clin Nutr 80:514–523

    CAS  PubMed  Google Scholar 

  19. Vandewalle S et al (2013) Bone size and bone strength are increased in obese male adolescents. J Clin Endocrinol Metab 98:3019–3028

    Article  CAS  PubMed  Google Scholar 

  20. Nagasaki K et al (2004) Obese Japanese children have low bone mineral density after puberty. J Bone Miner Metab 22:376–381

    Article  PubMed  Google Scholar 

  21. Rogol AD, Roemmich JN, Clark PA (2002) Growth at puberty. J Adolesc Health 31:192–200

    Article  PubMed  Google Scholar 

  22. Wang Y (2002) Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls. Pediatrics 110:903–910

    Article  PubMed  Google Scholar 

  23. Pollock NK et al (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86:1530–1538

    CAS  PubMed  Google Scholar 

  24. Rhie YJ et al (2010) Effects of body composition, leptin, and adiponectin on bone mineral density in prepubertal girls. J Korean Med Sci 25:1187–1190

    Article  PubMed Central  PubMed  Google Scholar 

  25. Shaikh MG et al (2014) The relationship between bone mass and body composition in children with hypothalamic and simple obesity. Clin Endocrinol (Oxf) 80:85–91

    Article  CAS  Google Scholar 

  26. Campos RM et al (2012) Influence of visceral and subcutaneous fat in bone mineral density of obese adolescents. Arq Bras Endocrinol Metab 56:12–18

    Google Scholar 

  27. Karlsson AK et al (2013) Measurements of total and regional body composition in preschool children: a comparison of MRI, DXA, and anthropometric data. Obesity (Silver Spring) 21:1018–1024

    Article  Google Scholar 

  28. Chung W, Lee J, Ryu O-H (2013) Is the negative relationship between obesity and bone mineral content greater for older women? J Bone Miner Metab 32:505–513

    Article  PubMed  Google Scholar 

  29. Laddu DR et al (2013) Longitudinal relationships between whole body and central adiposity on weight-bearing bone geometry, density, and bone strength: a pQCT study in young girls. Arch Osteoporos 8:156

    Article  PubMed Central  PubMed  Google Scholar 

  30. Dimitri P, Wales J, Bishop N (2011) Adipokines, bone-derived factors and bone turnover in obese children; evidence for altered fat-bone signalling resulting in reduced bone mass. Bone 48:189–196

    Article  CAS  PubMed  Google Scholar 

  31. Cao JJ (2011) Effects of obesity on bone metabolism. J Orthop Surg Res 6:30

    Article  PubMed Central  PubMed  Google Scholar 

  32. Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res 17:1563–1569

    Article  CAS  PubMed  Google Scholar 

  33. Do Prado WL et al (2009) Relationship between bone mineral density, leptin and insulin concentration in Brazilian obese adolescents. J Bone Miner Metab 27:613–619

    Article  CAS  PubMed  Google Scholar 

  34. Ducy P et al (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100:197–207

    Article  CAS  PubMed  Google Scholar 

  35. Kohlboeck G et al (2014) Peer problems are associated with elevated serum leptin levels in children. Psychol Med 44:255–265

    Article  PubMed  Google Scholar 

  36. Sominsky L, Spencer SJ (2014) Eating behavior and stress: a pathway to obesity. Front Psychol 5:434

    Article  PubMed Central  PubMed  Google Scholar 

  37. Bonnet N, Courteix D, Benhamou CL (2005) Leptin, central nervous system, and bone: influence of physical activity. Jt Bone Spine 72:477–480

    Article  Google Scholar 

  38. Kajimura D et al (2013) Adiponectin regulates bone mass via opposite central and peripheral mechanisms through FoxO1. Cell Metab 17:901–915

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Mohiti-Ardekani J et al (2014) Relationships between serum adipocyte hormones (adiponectin, leptin, resistin), bone mineral density and bone metabolic markers in osteoporosis patients. J Bone Miner Metab 32:400–404

    Article  CAS  PubMed  Google Scholar 

  40. Abseyi N et al (2012) Relationships between osteocalcin, glucose metabolism, and adiponectin in obese children: is there crosstalk between bone tissue and glucose metabolism? J Clin Res Pediatr Endocrinol 4:182–188

    Article  PubMed Central  PubMed  Google Scholar 

  41. Rochefort GY et al (2011) Osteocalcin–insulin relationship in obese children: a role for the skeleton in energy metabolism. Clin Endocrinol (Oxf) 75:265–270

    Article  CAS  Google Scholar 

  42. Capulli M, Paone R, Rucci N (2014) Osteoblast and osteocyte: games without frontiers. Arch Biochem Biophys 561:3–12

    Article  CAS  PubMed  Google Scholar 

  43. Wolf G (2008) Energy regulation by the skeleton. Nutr Rev 66:229–233

    Article  PubMed  Google Scholar 

  44. Garanty-Bogacka B et al (2013) Association between serum osteocalcin, adiposity and metabolic risk in obese children and adolescents. Endokrynol Pol 64:346–352

    Article  CAS  PubMed  Google Scholar 

  45. Schafer AL et al (2011) Change in undercarboxylated osteocalcin is associated with changes in body weight, fat mass, and adiponectin: parathyroid hormone (1–84) or alendronate therapy in postmenopausal women with osteoporosis (the PaTH study). J Clin Endocrinol Metab 96:E1982–E1989

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Yang S et al (2011) Foxo1 mediates insulin-like growth factor 1 (IGF1)/insulin regulation of osteocalcin expression by antagonizing Runx2 in osteoblasts. J Biol Chem 286:19149–19158

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  47. Morse A et al (2014) Mechanical load increases in bone formation via a sclerostin-independent pathway. J Bone Miner Res 29:2456–2467

    Article  CAS  PubMed  Google Scholar 

  48. Williams BO, Insogna KL (2009) Where Wnts went: the exploding field of Lrp5 and Lrp6 signaling in bone. J Bone Miner Res 24:171–178

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Turner CH et al (2009) Mechanobiology of the skeleton. Sci Signal 2:pt3

    Article  PubMed Central  PubMed  Google Scholar 

  50. Armamento-Villareal R et al (2012) Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. J Bone Miner Res 27:1215–1221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  51. Campos RM et al (2012) The role of pro/anti-inflammatory adipokines on bone metabolism in NAFLD obese adolescents: effects of long-term interdisciplinary therapy. Endocrine 42:146–156

    Article  CAS  PubMed  Google Scholar 

  52. Campos R et al (2013) Interaction of bone mineral density, adipokines and hormones in obese adolescents girls submitted in an interdisciplinary therapy. J Pediatr Endocrinol Metab 26:663–668

    Article  CAS  PubMed  Google Scholar 

  53. Reinehr T, Roth C (2010) A new link between skeleton, obesity and insulin resistance: relationships between osteocalcin, leptin and insulin resistance in obese children before and after weight loss. Int J Obes 34:852–858

    Article  CAS  Google Scholar 

  54. Stettler N et al (2008) Observational study of bone accretion during successful weight loss in obese adolescents. Obesity (Silver Spring) 16:96–101

    Article  Google Scholar 

  55. Campos RM et al (2014) Aerobic plus resistance training improves bone metabolism and inflammation in adolescents who are obese. J Strength Cond Res 28:758–766

    Article  PubMed  Google Scholar 

  56. Gajewska J et al (2013) Alterations in markers of bone metabolism and adipokines following a 3-month lifestyle intervention induced weight loss in obese prepubertal children. Exp Clin Endocrinol Diabetes 121:498–504

    Article  CAS  PubMed  Google Scholar 

  57. Blüher S et al (2014) Effects of a 1-year exercise and lifestyle intervention on irisin, adipokines, and inflammatory markers in obese children. Obesity 22:1701–1708

    Article  PubMed  Google Scholar 

  58. Broom DR et al (2007) Exercise-induced suppression of acylated ghrelin in humans. J Appl Physiol (1985) 102:2165–2171

    Article  CAS  Google Scholar 

  59. Khan K (2001) Physical activity and bone health. Human Kinetics 1

  60. Ka K et al (2013) Association between lean and fat mass and indicators of bone health in prepubertal Caucasian children. Horm Res Paediatr 80:154–162

    Article  CAS  PubMed  Google Scholar 

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Conflict of interest

All authors have no conflicts of interest.

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Authors and Affiliations

  1. Laboratory of the Metabolic Adaptations to Exercise under Physiological and Pathological Conditions (AME2P), EA 3533, Clermont University, Blaise Pascal University, Clermont-Ferrand, France

    Elodie Chaplais, David Thivel, Frederic Dutheil, Pascale Duche & Daniel Courteix

  2. School of Exercise Science, Australian Catholic University, Strathfield campus, Locked Bag 2002, Strathfield, NSW, 2135, Australia

    Elodie Chaplais, David Greene, Frederic Dutheil, Geraldine Naughton & Daniel Courteix

  3. CRNH-Auvergne, Clermont-Ferrand, France

    David Thivel, Pascale Duche & Daniel Courteix

  4. Occupational Medicine, University Hospital CHU G. Montpied, 63000, Clermont-Ferrand, France

    Frederic Dutheil

  5. School of Exercise Science, Australian Catholic University, Melbourne campus, Fitzroy MDC, Locked Bag 4115, Fitzroy, VIC, 3065, Australia

    Geraldine Naughton

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  1. Elodie Chaplais
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  2. David Thivel
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  4. Frederic Dutheil
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  7. Daniel Courteix
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Correspondence to Elodie Chaplais.

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Chaplais, E., Thivel, D., Greene, D. et al. Bone-adiposity cross-talk: implications for pediatric obesity. J Bone Miner Metab 33, 592–602 (2015). https://doi.org/10.1007/s00774-015-0654-6

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  • DOI: https://doi.org/10.1007/s00774-015-0654-6

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